The mating system affects the temperature sensitivity of male and female fertility

1. To mitigate effects of climate change it is important to understand
species’ responses to increasing temperatures. This has often been done by
studying survival or activity at temperature extremes. Before such
extremes are reached, however, effects on fertility may already be
apparent. 2. Sex differences in the thermal sensitivity of fertility (TSF)
could impact species persistence under climate warming because female
fertility is typically more limiting to population growth than male
fertility. However, little is known about sex differences in TSF. 3. Here
we first demonstrate that the mating system can strongly influence TSF
using the seed beetle Callosobruchus maculatus. We exposed populations
carrying artificially induced mutations to two generations of short-term
experimental evolution under alternative mating systems, manipulating the
opportunity for natural and sexual selection on the mutations. We then
measured TSF in males and females subjected to juvenile or adult heat
stress. 4. Populations kept under natural and sexual selection had higher
fitness, but similar TSF, compared to control populations kept under
relaxed selection. However, females had higher TSF than males, and
strikingly, this sex difference had increased over only two generations in
populations evolving under sexual selection. 5. We hypothesized that an
increase in male-induced harm to females during mating had played a
central role in driving this evolved sex difference, and indeed, remating
under conditions limiting male harassment of females reduced both male and
female TSF. Moreover, we show that manipulation of mating system
parameters in C. maculatus generates intraspecific variation in the sex
difference in TSF equal to that found among a diverse set of studies on
insects. 6. Our study provides a causal link between the mating system and
TSF. Sexual conflict, (re)mating rates, and genetic responses to sexual
selection differ among ecological settings, mating systems and species.
Our study therefore also provides mechanistic understanding for the
variability in previously reported TSFs which can inform future
experimental assays and predictions of species responses to climate
warming.

1. 为缓解气候变化带来的影响，理解物种对温度升高的响应至关重要。过往相关研究多聚焦于极端温度下的物种存活或活动情况。然而，在极端温度来临之前，温度对物种生育能力的影响或许已显现。
2. 生育温度敏感性（thermal sensitivity of fertility, TSF）的性别差异可能会影响气候变暖下的物种存续——由于雌性生育能力对种群增长的限制作用通常强于雄性。但目前学界对TSF的性别差异仍知之甚少。
3. 本研究首先以四纹豆象（Callosobruchus maculatus）为实验对象，证明交配系统可对TSF产生强烈调控作用。我们将携带人工诱导突变的种群置于不同交配系统下开展为期两代的短期实验进化，同时操控针对这些突变的自然选择与性选择机会。随后，我们分别测定了经历幼虫期或成虫期热胁迫的雌雄个体的TSF。
4. 与维持松弛选择的对照种群相比，经历自然选择与性选择的种群具有更高的适合度，但二者的TSF并无显著差异。不过，雌性的TSF显著高于雄性；尤为引人注目的是，在仅经过两代性选择演化的种群中，这种TSF的性别差异显著扩大。
5. 我们提出假说：交配过程中雄性对雌性造成的伤害加剧，是驱动这一演化而来的TSF性别差异的核心因素。实验结果证实，在限制雄性对雌性骚扰的条件下进行再次交配，可同时降低雌雄个体的TSF。此外，我们发现，对四纹豆象的交配系统参数进行操控，可使其TSF的性别差异产生种内变异，该变异幅度与已发表的各类昆虫相关研究中的差异水平相当。
6. 本研究建立了交配系统与TSF之间的因果关联。性冲突、（再次）交配频率以及对性选择的遗传响应，会因生态环境、交配系统以及物种的不同而存在差异。因此，本研究也为既往报道的TSF研究结果的异质性提供了机制层面的解释，可为未来的实验测定以及物种对气候变暖响应的预测工作提供参考。